Immunogenic HLA-B*0702-restricted epitopes derived from human telomerase reverse transcriptase that elicit antitumor cytotoxic T-cell responses

Clinical Cancer Research

Volumn 12, Issue 10, 2006, Pages 3158-3167

  Adotévi, Olivier ^a,c,f   Mollier, Karine ^b   Neuveut, Christine ^a   Cardinaud, Sylvain ^c   Boulanger, Emmanuelle ^c   Mignen, Blandine ^d   Fridman, Wolf Hervé ^a   Zanetti, Maurizio ^e   Charneau, Pierre ^b   Tartour, Eric ^a   Lemonnier, François ^c   Langlade Demoyen, Pierre ^c  

^a INSERM   (France)

^b Unité de Virologie Moléculaire   (France)

^c INSTITUT PASTEUR   (France)

^d ETABLISSEMENT FRANÇAIS DU SANG   (France)

^e UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

^f HÔPITAL EUROPÉEN GEORGES POMPIDOU   (France)

Author keywords

[No Author keywords available]

Indexed keywords

EPITOPE; HLA B ANTIGEN; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 1; PEPTIDES AND PROTEINS; PROTEIN P1; PROTEIN P277; PROTEIN P342; PROTEIN P351; PROTEIN P4; PROTEIN P68; TELOMERASE REVERSE TRANSCRIPTASE; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANTINEOPLASTIC ACTIVITY; ARTICLE; CANCER IMMUNOTHERAPY; CONTROLLED STUDY; CYTOTOXIC T LYMPHOCYTE; HUMAN; HUMAN CELL; IMMUNOGENICITY; IN VITRO STUDY; IN VIVO STUDY; MAJOR HISTOCOMPATIBILITY COMPLEX; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; TUMOR CELL;

ANIMALS; CANCER VACCINES; CELL LINE; DNA; DNA-BINDING PROTEINS; EPITOPES, T-LYMPHOCYTE; HLA-B ANTIGENS; HUMANS; IMMUNOTHERAPY; MICE; MICE, TRANSGENIC; NEOPLASMS; PEPTIDE FRAGMENTS; PLASMIDS; TELOMERASE; VACCINATION; VACCINES, SYNTHETIC;

EID: 33744810308     PISSN: 10780432     EISSN: None     Source Type: Journal    
DOI: 10.1158/1078-0432.CCR-05-2647     Document Type: Article

References (50)

1. Vonderheide RH. Telomerase as a universal tumor-associated antigen for cancer immunotherapy. Oncogene 2002;21:674-9.
2. Zanetti M, Hernandez X, Langlade-Demoyen P. Telomerase reverse transcriptase as target for anti-tumor T cell responses in humans. Springer Semin Immunopathol 2005;27:87-104.
3. Harrington L, McPhail T, Mar V, et al. A mammalian telomerase-associated protein. Science 1997;275: 973-7.
4. Nakamura TM, Morin GB, Chapman KB, et al. Telomerase catalytic subunit homology from fission yeast and human. Science 1997;277:955-99.
5. Kim NW, Piatyszek MA, Prowse KR, et al. Specific association of human telomerase activity with immortal cells and cancer. Science 1994;266:2011-5.
6. Janknecht R. On the road to immortality; hTERT up regulation in cancer cells. FEBS Lett 2004;564:9-13.
7. Counter CM, Gupta J, Harley CB, Leber B, Bacchetti S. Telomerase activity in normal leukocytes and in hematologic malignancies. Blood 1995;85:2315-20.
8. Weng NP, Granger L, Modes RJ. Telomere lengthening and telomerase activation during human B cell differentiation. Proc Natl Acad Sci U S A 1997;94:10827-32.
9. Hahn WC, Stewart SA, Brooks MW, et al. Inhibition of telomerase limits the growth of human cancer cells. Nat Med 1999;5:1164-70.
10. Boon T, van der Bruggen P. Human tumor antigens recognized by T lymphocytes. J Exp Med 1996;183: 725-9.
11. Rosenberg SA. A new era for cancer immunotherapy based on the genes that encode cancer antigens. Immunity 1999;10:281-7.
12. Vonderheide RH, Hahn WC, Schultze JL, Nadler LM. The telomerase catalytic subunit is a widely expressed tumor-associated antigen recognized by cytotoxic T lymphocytes. Immunity 1999;10:673-9.
13. Minev B, Hipp J, Firat H, Schmidt JD, Langlade-Demoyen P, Zanetti M. Cytotoxic T cell immunity against telomerase reverse transcriptase in humans. Proc Natl Acad Sci U S A 2000;97:4796-801.
14. Hernandez J, Garcia-Pons F, Lone YC, et al. Identification of a human telomerase reverse transcriptase peptide of low affinity for HLA-A2.1 that induces cytotoxic T lymphocytes and mediates lysis of tumor cells. Proc Natl Acad Sci U S A 2002;99:12275-80.
15. Titu LV, Loveday RL, Madden LA, Cawkwell L, Monson JR, Greenman J. Cytotoxic T-cell immunity against telomerase reverse transcriptase in colorectal cancer patients. Oncol Rep 2004;12:871-6.
16. Amarnath SM, Dyer CE, Ramesh A, Iwuagwu O, Drew PJ, Greenman J. In vitro quantification of the cytotoxic T lymphocyte response against human telomerase reverse transcriptase in breast cancer. Int J Oncol 2004;25:211-7.
17. Gannagé M, Abel M, Michallet AS, et al. Ex vivo characterization of multiepitopic tumor-specific CDS Tcells in patients with chronic myeloid leukemia: implications for vaccine development and adoptive cellular immunotherapy. J Immunol 2005;174:8210-8.
18. + T lymphocytes in patients with cancer. Blood 2006;107:1505-12.
19. + T lymphocytes. Clinical Cancer Res 2004;10:828-39.
20. Parkhurst MR, Riley JP, Igarashi T, Li Y, Robbins PF, Rosenberg SA. Immunization of patients with the hTERT:540-548 peptide induces peptide-reactive T lymphocytes that do not recognize tumors endogenously expressing telomerase. Clin Cancer Res 2004;10:4688-98.
21. Krausa P, Brywka M III, Savage D, et al. Genetic polymorphism within HLA-A*02: significant allelic variation revealed in different populations. Tissue Antigens 1995;45:223-31.
22. Vonderheide RH, Anderson KS, Hahn WC, Butler MO, Schultze JL, Nadler LM. Characterization of HLA-A3-restricted cytotoxic T lymphocytes reactive against the widely expressed tumor antigen telomerase. Clin Cancer Res 2001;7:3343-8.
23. Arai J, Yasukawa M, Ohminami H, Kakimoto M, Hasegawa A, Fujita S. Identification of human telomerase reverse transcriptase-derived peptides that induce HLA-A24-restricted antileukemia cytotoxic T lymphocytes. Blood 2001;9:2903-7.
24. Schreurs MW, Kueter EW, Scholten KB, Kramer D, Meijer CJ, Hooijberg E. Identification of a potential human telomerase reverse transcriptase-derived, HLA-A1-restricted cytotoxic T lymphocyte epitope. Cancer Immunol Immunother 2005;54:703-12.
25. + T-helper cells. Cancer Res 2002;62:2600-5.
26. Schroers R, Shen L, Rollins L, et al. Human telomerase reverse transcriptase-specific T-helper responses induced by promiscuous major histocompatibility complex class II-restricted epitopes. Clin Cancer Res 2003;9:4743-55.
27. Erratum in: Clin Cancer Res 2004;10:3576.
28. Voorter CE, van der Vlies SA, van den Berg-Loonen EM. Sequence-based typing of HLA-B: the B7 cross-reacting group. Tissue Antigens 2000: 56:356-62
29. Rohrlich PS, Cardinaud S, Firat H, et al. HLA-B*0702 Transgenic, H-2KbDb double-knockout mice: phenotypical and functional characterization in response to influenza virus. Int Immunol 2003;15:765-72.
30. Smith KD, Lutz CT. Peptide-dependent expression of HLA-B7 on antigen processing-deficient T2 cells. J Immunol 1996;156:3755-64.
31. Morand P, Buisson M, Collandre H, et al. Human herpesvirus 8 and Epstein Barr-virus in a cutaneous B-cell lymphoma and a malignant cell line established from the blood of an AIDS patient. Leuk Lymphoma 1999;35:379-87.
32. Cardinaud S, Moris A, Fevrier M, et al. Identification of cryptic MHC I-restricted epitopes encoded by HIV-1 alternative reading frames. J Exp Med 2004;199: 1053-63.
33. Rammensee H, Bachmann J, Emmerich NP, Bachor OA, Stevanovic S. SYFPEITHI: database for MHC ligands and peptide motifs. Immunogenetics 1999;50:213-9.
34. Liu K, Hodes RJ, Weng Np. Cutting edge: telomerase activation in human T lymphocytes does not require increase in telomerase reverse transcriptase (hTERT) protein but is associated with hTERT phosphorylation and nuclear translocation. J Immunol 2001;166:4826-30.
35. Frolkis M, Fischer MB, Wang Z, Lebkowski JS, Chiu CP, Majumdar AS. Dendritic cells reconstituted with human telomerase gene induce potent cytotoxic T-cell response against different types of tumors. Cancer Gene Ther 2003;1:239-49.
36. Firat H, Garcia-Pons F, Tourdot S, et al. H-2 class I knockout, HLA-A2.1-transgenic mice: a versatile animal model for preclinical evaluation of antitumor immunotherapeutic strategies. Eur J Immunol 1999;29:3112-21.
37. Counter CM, Hahn WC, Wei W, et al. Dissociation among in vitro telomerase activity, telomere maintenance, and cellular immortalization. Proc Natl Acad Sci U S A 1998;95:14723-8.
38. Loirat D, Lemonnier FA, Michel ML. Multiepitopic HLA-A*0201- restricted immune response against hepatitis B surface antigen after DNA-based immunization. J Immunol 2000;165:4748-55.
39. Sette A, Vitiello A, Reherman B, et al. The relationship between class I binding affinity and immunogenicity of potential cytotoxic T cell epitopes. J Immunol 1994;153:5586-92.
40. Sidney J, Southwood S, del Guercio MF, et al. Specificity and degeneracy in peptide binding to HLA-B7-like class I molecules. J Immunol 1996;157: 3480-90.
41. Sette A, Sidney J, Livingston BD, et al. Class I molecules with similar peptide-binding specificities are the result of both common ancestry and convergent evolution. Immunogenetics 2003;54:830-41.
42. Uebel S, Tampe R. Specificity of the proteasome and the TAP transporter. Curr Opin Immunol 1999;11: 203-8.
43. Van den Eynde BJ, Morel S. Differential processing of class-I-restricted epitopes by the standard proteasome and the immunoproteasome. Curr Opin Immunol 2001;13:147-53.
44. Morel S, Levy F, Burlet-Schiltz O, et al. Processing of some antigens by the standard proteasome but not by the immunoproteasome results in poor presentation by dendritic cells. Immunity 2000;12:107-17.
45. Schultz ES, Chapiro J, Lurquin C, et al. The production of a new MAGE-3 peptide presented to cytolytic T lymphocytes by HLA-B40 requires the immunoproteasome. J Exp Med 2002;195:391-9.
46. Rock KL, Goldberg AL. Degradation of cell proteins and the generation of MHC class I-presented peptides. Annu Rev Immunol 1999;17:739-79.
47. Tajima K, Ito Y, Demachi A, et al. Interferon-γ differentially regulates susceptibility of lung cancer cells to telomerase-specific cytotoxic T lymphocytes. Int J Cancer 2004;110:403-12.
48. Vonderheide RH, Schultze JL, Anderson KS, et al. Equivalent induction of telomerase-specific cytotoxic T lymphocytes from tumor-bearing patients and healthy individuals. Cancer Res 2001;61:8366-70.
49. Van der Burg SH, Visseren MJ, Brandt RM, Kast WM, Melief CJ. Immunogenicity of peptides bound to MHC class I molecules depends on the MHC-peptide complex stability. J Immunol 1996;156: 3308-14
50. + T cell responses in patients with metastatic prostate cancer. J Immunol 2005;174:3798-807.